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Genomes of the "Candidatus Actinomarinales" Order: Highly Streamlined Marine Epipelagic Actinobacteria.

ABSTRACT: "Candidatus Actinomarinales" was defined as a subclass of exclusively marine Actinobacteria with small cells and genomes. We have collected all the available genomes in databases to assess the diversity included in this group and analyzed it by comparative genomics. We have found the equivalent of five genera and 18 genomospecies. They have genome reduction parameters equal to those of freshwater actinobacterial "Candidatus Nanopelagicales" or marine alphaproteobacterial Pelagibacterales Genome recruitment shows that they are found only in the photic zone and mainly in surface waters, with only one genus that is found preferentially at or below the deep chlorophyll maximum. "Ca Actinomarinales" show a highly conserved core genome (80% of the gene families conserved for the whole order) with a saturation of genomic diversity of the flexible genome at the genomospecies level. We found only a flexible genomic island preserved throughout the order; it is related to the sugar decoration of the envelope and uses several tRNAs as hot spots to increase its genomic diversity. Populations had a discrete level of sequence diversity similar to other marine microbes but drastically different from the much higher levels found for Pelagibacterales Genomic analysis suggests that they are all aerobic photoheterotrophs with one type 1 rhodopsin and a heliorhodopsin. Like other actinobacteria, they possess the F420 coenzyme biosynthesis pathway, and its lower reduction potential could provide access to an increased range of redox chemical transformations. Last, sequence analysis revealed the first "Ca Actinomarinales" phages, including a prophage, with metaviromic islands related to sialic acid cleavage.IMPORTANCE Microbiology is in a new age in which sequence databases are primary sources of information about many microbes. However, in-depth analysis of environmental genomes thus retrieved is essential to substantiate the new knowledge. Here, we study 182 genomes belonging to the only known exclusively marine pelagic group of the phylum Actinobacteria The aquatic branch of this phylum is largely known from environmental sequencing studies (single-amplified genomes [SAGs] and metagenome-assembled genomes [MAGs]), and we have collected and analyzed the available information present in databases about the "Ca. Actinomarinales." They are among the most streamlined microbes to live in the epipelagic zone of the ocean, and their study is critical to obtain a proper view of the diversity of Actinobacteria and their role in aquatic ecosystems.

SUBMITTER: Lopez-Perez M

PROVIDER: S-EPMC7771536 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Bacteria often respond to environmental stimuli using transcriptional control, but this may not be the case for marine bacteria such as "Candidatus Pelagibacter ubique," a cultivated representative of the SAR11 clade, the most abundant organism in the ocean. This bacterium has a small, streamlined genome and an unusually low number of transcriptional regulators, suggesting that transcriptional control is low in Pelagibacter and limits its response to environmental conditions. Transcriptome sequencing during batch culture growth revealed that only 0.1% of protein-encoding genes appear to be under transcriptional control in Pelagibacter and in another oligotroph (SAR92) whereas >10% of genes were under transcriptional control in the copiotrophs Polaribacter sp. strain MED152 and Ruegeria pomeroyi When growth levels changed, transcript levels remained steady in Pelagibacter and SAR92 but shifted in MED152 and R. pomeroyi Transcript abundances per cell, determined using an internal RNA sequencing standard, were low (<1 transcript per cell) for all but a few of the most highly transcribed genes in all four taxa, and there was no correlation between transcript abundances per cell and shifts in the levels of transcription. These results suggest that low transcriptional control contributes to the success of Pelagibacter and possibly other oligotrophic microbes that dominate microbial communities in the oceans.Diverse heterotrophic bacteria drive biogeochemical cycling in the ocean. The most abundant types of marine bacteria are oligotrophs with small, streamlined genomes. The metabolic controls that regulate the response of oligotrophic bacteria to environmental conditions remain unclear. Our results reveal that transcriptional control is lower in marine oligotrophic bacteria than in marine copiotrophic bacteria. Although responses of bacteria to environmental conditions are commonly regulated at the level of transcription, metabolism in the most abundant bacteria in the ocean appears to be regulated by other mechanisms.

Project description:The genomes of four novel marine Actinobacteria have been assembled from large metagenomic data sets derived from the Mediterranean deep chlorophyll maximum (DCM). These are the first marine representatives belonging to the order Acidimicrobiales and only the second group of planktonic marine Actinobacteria to be described. Their streamlined genomes and photoheterotrophic lifestyle suggest that they are planktonic, free-living microbes. A novel rhodopsin clade, acidirhodopsins, related to freshwater actinorhodopsins, was found in these organisms. Their genomes suggest a capacity to assimilate C2 compounds, some using the glyoxylate bypass and others with the ethylmalonyl-coenzyme A (CoA) pathway. They are also able to derive energy from dimethylsulfopropionate (DMSP), sulfonate, and carbon monoxide oxidation, all commonly available in the marine habitat. These organisms appear to be prevalent in the deep photic zone at or around the DCM. The presence of sister clades to the marine Acidimicrobiales in freshwater aquatic habitats provides a new example of marine-freshwater transitions with potential evolutionary insights. Despite several studies showing the importance and abundance of planktonic Actinobacteria in the marine habitat, a representative genome was only recently described. In order to expand the genomic repertoire of marine Actinobacteria, we describe here the first Acidimicrobidae genomes of marine origin and provide insights about their ecology. They display metabolic versatility in the acquisition of carbon and appear capable of utilizing diverse sources of energy. One of the genomes harbors a new kind of rhodopsin related to the actinorhodopsin clade of freshwater origin that is widespread in the oceans. Our data also support their preference to inhabit the deep chlorophyll maximum and the deep photic zone. This work contributes to the perception of marine actinobacterial groups as important players in the marine environment with distinct and important contributions to nutrient cycling in the oceans.

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Genomes of the "Candidatus Actinomarinales" Order: Highly Streamlined Marine Epipelagic Actinobacteria.

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